Tsetse fly

Tsetse flies can be seen as independent individuals in two forms: as third-instar larvae, and as adults.

Tsetse first become separate from their mothers during the third larval instar, during which they have the typical appearance of maggots. However, this life stage is short, lasting at most a few hours, and is almost never observed outside of the laboratory.

Tsetse next develop a hard external case, the puparium, and become pupae—small, hard-shelled, oblongs with two distinctive, small, dark lobes at the tail (breathing) end. Tsetse pupae are under 1 cm long.[9] Within the puparial shell, tsetse complete the last two larval instars and the pupal stage.

At the end of the pupal stage, tsetse emerge as adult flies. The adults are relatively large flies, with lengths of 0.5-1.5 cm,[9] and have a recognizable shape or bauplan which makes them easy to distinguish from other flies. Tsetse have large heads, distinctly separated eyes, and unusual antennae. The thorax is quite large, while the abdomen is wide rather than elongated and shorter than the wings.

Four characteristics definitively separate adult tsetse from other kinds of flies:

Proboscis	Tsetse have a distinct proboscis, a long thin structure attached to the bottom of the head and pointing forward.	A photograph of the head of a tsetse illustrating the forward pointing proboscis
Folded wings	When at rest, tsetse fold their wings completely one on top of the other.	A photograph of the whole body of a tsetse illustrating the folded wings when at rest
Hatchet cell	The discal medial ("middle") cell of the wing has a characteristic hatchet shape resembling a meat cleaver or a hatchet.	A photograph of the wing of a tsetse illustrating the hatchet shaped central cell
Branched arista hairs	The antennae have arista with hairs which are themselves branched.	A photograph and diagram of the head of a tsetse illustrating the branched hairs of the antenna's arista

Like all other insects, tsetse flies have an adult body comprising three visibly distinct parts: the head, the thorax and the abdomen.

The head has large eyes, distinctly separated on each side, and a distinct, forward-pointing proboscis attached underneath by a large bulb. The thorax is large, made of three fused segments. Three pairs of legs are attached to the thorax, as are two wings and two halteres. The abdomen is short but wide and changes dramatically in volume during feeding.

The internal anatomy of tsetse is fairly typical of the insects. The crop is large enough to accommodate a huge increase in size during the bloodmeal since tsetse can take a bloodmeal equal in weight to themselves. The reproductive tract of adult females includes a uterus which can become large enough to hold the third-instar larva at the end of each pregnancy. The article Parasitic flies of domestic animals has a diagram of anatomy of dipteran flies.

Most tsetse flies are physically very tough. Houseflies are easily killed with a flyswatter, but a great deal of effort is needed to crush a tsetse fly.

Glossina palpalis and G. morsitans from a 1920 lexicon

Tsetse have an unusual lifecycle which may be due to the richness of their food source. A female fertilizes only one egg at a time and retains each egg within her uterus to have the offspring develop internally during the first three larval stages, a method called adenotrophic viviparity. During this time, the female feeds the developing offspring with a milky substance secreted by a modified gland in the uterus.[10] In the third larval stage, the tsetse larva leaves the uterus and begins its independent life. The newly independent tsetse larva crawls into the ground, and develops a hard outer shell called the puparial case, in which it completes its morphological transformation into an adult fly.

This lifestage has a variable duration, generally 20 to 30 days, and the larva must rely on stored resources during this time. The importance of the richness of blood to this development can be seen, since all tsetse development before it emerges from the puparial case as a full adult occurs without feeding, based only on nutritional resources provided by the female parent. The female must get enough energy for her needs, for the needs of her developing offspring, and for the stored resources which her offspring will require until it emerges as an adult.

Technically, these insects undergo the standard development process of insects, which consists of oocyte formation, ovulation, fertilization, development of the egg, three larval stages, a pupal stage, and the emergence and maturation of the adult.

The genome of Glossina morsitans was sequenced in 2014.[11]

Tsetse flies have three known symbionts. The primary symbiont is Wigglesworthia within the fly's bacteriocytes, the secondary symbiont is Sodalis intercellularly or intracellularly, and the third is some kind of Wolbachia.[12][13]

The tsetse genus is generally split into three groups of species based on a combination of distributional, behavioral, molecular and morphological characteristics. The genus includes:

Cows dead from rinderpest in South Africa, 1896

The depopulated and apparently primevally wild Africa seen in wildlife documentary films was formed in the 19th century by disease, a combination of rinderpest and the tsetse fly. In 1887, the rinderpest virus was accidentally imported in livestock brought by an Italian expeditionary force to Eritrea. It spread rapidly, reaching Ethiopia by 1888, the Atlantic coast by 1892 and South Africa by 1897. Rinderpest, a cattle plague from central Asia, killed over 90% of the cattle of the pastoral peoples such as the Masai of east Africa. With no native immunity, most of the population – some 5.5 million cattle – died in southern Africa. Pastoralists were left with no animals - their source of income; and farmers were deprived of their working animals for ploughing and irrigation. The pandemic coincided with a period of drought, causing widespread famine. The starving human populations died of smallpox, cholera, typhoid and diseases imported from Europe. It's estimated that two-thirds of the Masai died in 1891. [6]

The land was left emptied of its cattle and its people, enabling the colonial powers Germany and Britain to take over Tanzania and Kenya with little effort. With greatly reduced grazing, grassland turned rapidly to bush. The closely cropped grass sward was replaced in a few years by woody grassland and thornbush, ideal habitat for tsetse flies. Wild mammal populations increased rapidly, accompanied by the tsetse fly. Highland regions of east Africa which had been free of tsetse fly were colonised by the pest, accompanied by sleeping sickness, until then unknown in the area. Millions of people died of the disease in the early 20th century. [6]

Serengeti National Park, Tanzania

The areas occupied by the tsetse fly were largely barred to animal husbandry. Sleeping sickness was dubbed "the best game warden in Africa" by conservationists, who assumed that the land, empty of people and full of game animals, had always been like that. Julian Huxley of the World Wildlife Fund called the plains of east Africa "a surviving sector of the rich natural world as it was before the rise of modern man". [6] They created numerous large reserves for hunting safaris. In 1909 the newly retired president Theodore Roosevelt went on a safari that brought over 10,000 animal carcasses to America. Later, much of the land was turned over to nature reserves and national parks such as the Serengeti, Masai Mara, Kruger and Okavango Delta. The result, across eastern and southern Africa, is a modern landscape of manmade ecosystems: farmland and pastoral land largely free of bush and tsetse fly; and bush controlled by the tsetse fly. [6]

Tsetse flies are regarded as a major cause of rural poverty in sub-Saharan Africa because they prevent mixed farming. The land infested with tsetse flies is often cultivated by people using hoes rather than more efficient draught animals because nagana, the disease transmitted by tsetse, weakens and often kills these animals. Cattle that do survive produce little milk, pregnant cows often abort their calves, and manure is not available to fertilize the worn-out soils.

Tsetse fly from Burkina Faso

The disease nagana or African animal trypanosomiasis (AAT) causes gradual health decline in infected livestock, reduces milk and meat production, and increases abortion rates. Animals eventually succumb to the disease (annual cattle deaths caused by trypanosomiasis are estimated at 3 million). This has an enormous impact on the livelihood of farmers who live in tsetse-infested areas, as infected animals cannot be used to plough the land, and keeping cattle is only feasible when the animals are kept under constant prophylactic treatment with trypanocidal drugs, often with associated problems of drug resistance, counterfeited drugs, and suboptimal dosage. The overall annual direct lost potential in livestock and crop production was estimated at US$4.5 billion.[15][16]

The tsetse fly lives in nearly 10,000,000 square kilometres (4,000,000 sq mi) in sub-Saharan Africa (mostly wet tropical forest) and many parts of this large area is fertile land that is left uncultivated—a so-called green desert not used by humans and cattle. Most of the 37 countries infested with tsetse are poor, debt-ridden and underdeveloped. Of the 39 tsetse-infested countries, 32 are low-income, food-deficit countries, 29 are least developed countries, and 30 are among the 40 most heavily indebted poor countries. Eradicating the tsetse and trypanosomiasis (T&T) problem would allow rural Africans to use these areas for animal husbandry or the cultivation of crops and hence increase food production. Only 45 million cattle, of 172 million present in sub-Saharan Africa, are kept in tsetse-infested areas but are often forced into fragile ecosystems like highlands or the semiarid Sahel zone, which increases overgrazing and overuse of land for food production.

In addition to this direct impact, the presence of tsetse and trypanosomiasis discourages the use of more productive exotic and cross-bred cattle, depresses the growth and affects the distribution of livestock populations, reduces the potential opportunities for livestock and crop production (mixed farming) through less draught power to cultivate land and less manure to fertilize (in an environment-friendly way) soils for better crop production, and affects human settlements (people tend to avoid areas with tsetse flies).

Tsetse flies transmit a similar disease to humans, called African trypanosomiasis - human African trypanosomiasis (HAT) or sleeping sickness. An estimated 70 million people in 20 countries are at different levels of risk[17] and only 3-4 million people are covered by active surveillance. The DALY index (disability-adjusted life years), an indicator to quantify the burden of disease, includes the impact of both the duration of life lost due to premature death and the duration of life lived with a disability. The annual burden of sleeping sickness is estimated at 2 million DALYs. Since the disease tends to affect economically active adults, the total cost to a family with a patient is about 25% of a year's income.[18]

The tsetse-vectored trypanosomiases affect various vertebrate species including humans, antelopes, bovine cattle, camels, horses, sheep, goats, and pigs. These diseases are caused by several different trypanosome species that may also survive in wild animals such as crocodiles and monitor lizards. The diseases have different distributions across the African continent, so are transmitted by different species. This table summarizes this information:[19][22]

Human African trypanosomiasis, also called sleeping sickness, is caused by trypanosomes of the species Trypanosoma brucei. This disease is invariably fatal unless treated but can almost always be cured with current medicines, if the disease is diagnosed early enough.

Sleeping sickness begins with a tsetse bite leading to an inoculation in the subcutaneous tissue. The infection moves into the lymphatic system, leading to a characteristic swelling of the lymph glands called Winterbottom's sign.[23] The infection progresses into the blood stream and eventually crosses into the central nervous system and invades the brain leading to extreme lethargy and eventually to death.

The species Trypanosoma brucei, which causes the disease, has often been subdivided into three subspecies that were identified based either on the vertebrate hosts which the strain could infect or on the virulence of the disease in humans. The trypanosomes infectious to animals and not to humans were named Trypanosoma brucei brucei. Strains that infected humans were divided into two subspecies based on their different virulences: Trypanosoma brucei gambiense was thought to have a slower onset and Trypanosoma brucei rhodesiense refers to strains with a more rapid, virulent onset. This characterization has always been problematic but was the best that could be done given the knowledge of the time and the tools available for identification. A recent molecular study using restriction fragment length polymorphism analysis suggests that the three subspecies are polyphyletic,[24] so the elucidation of the strains of T. brucei infective to humans requires a more complex explanation. Procyclins are proteins developed in the surface coating of trypanosomes whilst in their tsetse fly vector.[25]

Other forms of human trypanosomiasis also exist but are not transmitted by tsetse. The most notable is American trypanosomiasis, known as Chagas disease, which occurs in South America, caused by Trypanosoma cruzi, and transmitted by certain insects of the Reduviidae, members of the Hemiptera.

Animal trypanosomiasis, also called nagana when it occurs in bovine cattle or horses or sura when it occurs in domestic pigs, is caused by several trypanosome species. These diseases reduce the growth rate, milk productivity, and strength of farm animals, generally leading to the eventual death of the infected animals. Certain species of cattle are called trypanotolerant because they can survive and grow even when infected with trypanosomes although they also have lower productivity rates when infected.

The course of the disease in animals is similar to the course of sleeping sickness in humans.

Trypanosoma congolense and Trypanosoma vivax are the two most important species infecting bovine cattle in sub-Saharan Africa. Trypanosoma simiae causes a virulent disease in swine.

Other forms of animal trypanosomiasis are also known from other areas of the globe, caused by different species of trypanosomes and transmitted without the intervention of the tsetse fly.

The tsetse fly vector ranges mostly in the central part of Africa.

Trypanosomiasis poses a considerable constraint on livestock agricultural development in Tsetse fly infested areas of sub Saharan Africa, especially in west and central Africa. International research conducted by ILRI in Nigeria, the Democratic Republic of the Congo and Kenya has shown that the N'Dama is the most resistant breed.  [26] [27]

Many techniques have reduced tsetse populations, with earlier, crude methods recently replaced by methods that are cheaper, more directed, and ecologically better.

One early technique involved slaughtering all the wild animals tsetse fed on. For example, the island of Principe off the west coast of Africa was entirely cleared of feral pigs in the 1930s, which led to the extirpation of the fly. While the fly eventually re-invaded in the 1950s, the new population of tsetse was free from the disease.

Another early technique involved complete removal of brush and woody vegetation from an area. Tsetse tend to rest on the trunks of trees so removing woody vegetation made the area inhospitable to the flies. However, the technique was not widely used and has been abandoned. Preventing regrowth of woody vegetation requires continuous clearing efforts, which is only practical where large human populations are present. The clearing of woody vegetation has come to be seen as an environmental problem more than a benefit.

Pesticides have been used to control tsetse starting initially during the early part of the twentieth century in localized efforts using the inorganic metal-based pesticides, expanding after the Second World War into massive aerial- and ground-based campaigns with organochlorine pesticides such as DDT applied as aerosol sprays at Ultra-Low Volume rates. Later, more targeted techniques used pour-on formulations in which advanced organic pesticides were applied directly to the backs of cattle.

Tsetse trap

Tsetse populations can be monitored and effectively controlled using simple, inexpensive traps. These often use electric blue cloth, since this color attracts the flies. Early traps mimicked the form of cattle but this seems unnecessary and recent traps are simple sheets or have a biconical form. The traps can kill by channeling the flies into a collection chamber or by exposing the flies to insecticide sprayed on the cloth. Tsetse are also attracted to large dark colors like the hides of cow and buffaloes. Some scientists put forward the idea that zebra have stripes, not as a camouflage in long grass, but because the black and white bands tend to confuse tsetse and prevent attack.[29][30]

The use of chemicals as attractants to lure tsetse to the traps has been studied extensively in the late 20th century, but this has mostly been of interest to scientists rather than as an economically reasonable solution. Attractants studied have been those tsetse might use to find food, like carbon dioxide, octenol, and acetone—which are given off in animals' breath and distributed downwind in an odor plume. Synthetic versions of these chemicals can create artificial odor plumes. A cheaper approach is to place cattle urine in a half gourd near the trap. For large trapping efforts, additional traps are generally cheaper than expensive artificial attractants.

A special trapping method is applied in Ethiopia, where the BioFarm Consortium (ICIPE, BioVision Foundation, BEA, Helvetas, DLCO-EA, Praxis Ethiopia) applies the traps in a sustainable agriculture and rural development context (SARD). The traps are just the entry point, followed by improved farming, human health and marketing inputs. This method is in the final stage of testing (as per 2006).

The sterile insect technique (SIT) is a form of pest control that uses ionizing radiation (gamma ray or X ray) to sterilize male flies that are mass-produced in special rearing facilities. The sterile males are released systematically from the ground or by air in tsetse-infested areas, where they mate with wild females, which do not produce offspring. As a result, this technique can eventually eradicate populations of wild flies. SIT is among the most environmentally friendly control tactics available, and is usually applied as the final component of an integrated campaign. It has been used to subdue the populations of many other fly species including the medfly, Ceratitis Capitata.

The sustainable removal of the tsetse fly is in many cases the most cost-effective way of dealing with the T&T problem resulting in major economic benefits for subsistence farmers in rural areas. Insecticide-based methods are normally very ineffective in removing the last remnants of tsetse populations, while, on the contrary, sterile males are very effective in finding and mating the last remaining females. Therefore, the integration of the SIT as the last component of an area-wide integrated approach is essential in many situations to achieve complete eradication of the different tsetse populations, particularly in areas of more dense vegetation.

A project that was implemented from 1994 to 1997 on the Island of Unguja, Zanzibar (United Republic of Tanzania), demonstrated that, after suppression of the tsetse population with insecticides, SIT completely removed the Glossina austeni Newstead population from the Island ([31]). The eradication of the tsetse fly from Unguja Island in 1997 was followed by the disappearance of the AAT which enabled farmers to integrate livestock keeping with cropping in areas where this had been impossible before. The increased livestock and crop productivity and the possibility of using animals for transport and traction significantly contributed to an increase in the quality of people's lives ([32][33]). A recent entomological survey (2015) jointly carried out by independent experts and the Department of Veterinary Services of Zanzibar has confirmed the tsetse-free status of the island, 18 years after eradication was declared.

In the Niayes region of Senegal, a coastal area close to Dakar, livestock keeping was difficult due to the presence of a population of Glossina palpalis gambiensis. Feasibility studies indicated that the fly population was confined to very fragmented habitats and a population genetics study indicated that the population was genetically isolated from the main tsetse belt in the south eastern part of Senegal. After completion of the feasibility studies (2006–2010), an area-wide integrated eradication campaign that included an SIT component was started in 2011, and by 2015, the Niayes region had become almost tsetse fly free.[34][35]

The entire target area (Block 1, 2 and 3) has a total surface of 1000 km2, and the first block (northern part) can be considered free of tsetse, as intensive monitoring has failed to detect since 2012 a single wild tsetse fly. The prevalence of AAT has decreased from 40-50% before the project started to less than 10% to date in blocks 1 and 2. Although insecticides are being used for fly suppression, they are applied for short periods on traps, nets and livestock, and are not spread into the environment. After the suppression activities are completed, no more insecticide is applied in the area. The removal of trypanosomosis will eliminate the need for constant prophylactic treatments of the cattle with trypanocidal drugs, therefore reducing residues of these drugs in the dung, meat and milk.

The main beneficiaries of the project are the many small holder farmers, the larger commercial farms and the consumers of meat and milk. According to a socio-economic survey and benefit cost analysis,[36] after eradication of the tsetse farmers will be able to replace their local breeds with improved breeds and increase their annual income by €2.8 million. In addition, it is expected that the number of cattle will be reduced by 45%, which will result in reduced environmental impacts.

• Buxton, P. (1955). The Natural History of Tsetse Flies: An Account of the Biology of the Genus Glossina (Diptera). London, UK: H.K. Lewis & Co.
• Ford, J. (1971). The Role of the Trypanosomiases in African Ecology. Oxford, UK: Clarendon Press.
• Glasgow, J. (1963). The Distribution and Abundance of Tsetse. International Series of Monographs on Pure and Applied Biology, No. 20. Oxford, UK: Pergamon Press.
• Leak, S. (1998). Tsetse Biology and Ecology: Their role in the Epidemiology and Control of Trypanosomiasis. New York: CABI Publishing. book site
• Maudlin, I., Holmes, P. H., and Miles, M. A. (2004). The Trypanosomiases. CAB International.
• McKelvey, J., Jr. (1973). Man Against Tsetse: Struggle for Africa. Ithaca, NY: Cornell University Press.
• Mulligan, H. & Potts, W. (1970). The African Trypanosomiases. London: George Allen and Unwin, Ltd.